Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light

Archives of Microbiology

Volumn 197, Issue 2, 2015, Pages 181-195

  Gorelova, Olga ^a   Baulina, Olga ^a   Solovchenko, Alexei ^a   Selyakh, Irina ^a   Chivkunova, Olga ^a   Semenova, Larisa ^a   Scherbakov, Pavel ^a   Burakova, Olga ^a   Lobakova, Elena ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Carbon partitioning; Chlorophyta; Micromorphometry; Stress; Symbiotic microalgae; Ultrastructure

Indexed keywords

NITROGEN; POLYSACCHARIDE; STARCH; CARBON; CHLOROPHYLL;

ALGAL CELL CULTURE; ALGAL GROWTH; ARTICLE; CELL COMPARTMENTALIZATION; CELL INCLUSION; CELL ULTRASTRUCTURE; CELL WALL; CHLOROPLAST; CONTROLLED STUDY; DESMODESMUS SP 3DP86E 1; GREEN ALGA; LIGHT STRESS; MICROALGA; NONHUMAN; OIL BODY; PHOTOCHEMICAL EFFICIENCY; PLASTID MEMBRANE; PRIORITY JOURNAL; STARVATION; SYMBIOSIS; THYLAKOID; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; RADIATION RESPONSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

CARBON; CELL WALL; CHLOROPHYLL; CHLOROPHYTA; LIGHT; MICROSCOPY, ELECTRON, TRANSMISSION; NITROGEN; PHOTOSYNTHESIS; SYMBIOSIS; THYLAKOIDS;

EID: 84925494221     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-014-1036-5     Document Type: Article

References (61)

1. Abe J, Kubo T, Takagi Y, Saito T, Miura K, Fukuzawa H, Matsuda Y (2004) The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii. Curr Genet 46:304–315. doi:10.1007/s00294-004-0526-4
2. Austin JR, Frost E, Vidi P-A, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703. doi:10.1105/tpc.105.039859
3. Barbato R, Friso G, Rigoni F, Dalla Vecchia F, Giacometti GM (1992) Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J Cell Biol 119:325–335
4. Baulina OI (2012) Ultrastructural plasticity of cyanobacteria. Springer, Berlin
5. Berner T, Izhaki I (1994) Effect of exogenous nitrogen levels on ultrastructure of zooxanthellae from the hermatypic coral Pocillopora damicornis. Pac Sci 48:254–262
6. Besagni C, Kessler F (2013) A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237:463–470. doi:10.1007/s00425-012-1813-9
7. Cunningham A, Maas P (1978) Time lag and nutrient storage effects in the transient growth response of Chlamydomonas reinhardii in nitrogen-limited batch and continuous culture. J Gen Microbiol 104:227–231. doi:10.1099/00221287-104-2-227
8. Davidi L, Katz A, Pick U (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta 236:19–33. doi:10.1007/s00425-011-1585-7
9. de Morais MG, Costa JAV (2007) Biofixation of carbon dioxide by Spirulina sp. and Scenedesmus obliquus cultivated in a three-stage serial tubular photobioreactor. J Biotechnol 129:439–445. doi:10.1016/j.jbiotec.2007.01.009
10. Dong H-P, Williams E, Wang D-Z, Xie Z-X, Hsia R-C, Jenck A, Halden R, Li J, Chen F, Place AR (2013) Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol 162:1110–1126. doi:10.1104/pp.113.214320
11. Dubinsky Z, Berman-Frank I (2001) Uncoupling primary production from population growth in photosynthesizing organisms in aquatic ecosystems. Aquat Sci-Res Across Boundaries 63:4–17
12. Fan J, Andre C, Xu C (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585:1985–1991. doi:10.1016/j.febslet.2011.11.001
13. Fernandes B, Teixeira J, Dragone G, Vicente AA, Kawano S, Bišová K, Přibyl P, Zachleder V, Vítová M (2013) Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour Technol 144:268–274. doi:10.1016/j.biortech.2013.06.096
14. Fisher T, Berner T, Iluz D, Dubinsky Z (1998) The kinetics of the photoacclimation response of Nannochloropsis sp. (Eustigmatophyceae): a study of changes in ultrastructure and PSU density. J Phycol 34:818–824
15. Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
16. García-Ferris C, Moreno J (1994) Oxidative modification and breakdown of ribulose-1, 5-bisphosphate carboxylase/oxygenase induced in Euglena gracilis by nitrogen starvation. Planta 193:208–215
17. García-Ferris C, de los Ríos A, Ascaso C, Moreno J (1996) Correlated biochemical and ultrastructural changes in nitrogen-starved Euglena gracilis. J Phycol 32:953–963. doi:10.1111/j.0022-3646.1996.00953.x
18. Geyer G (1973) Ultrahistochemie. Histochemische Arbeitsvorschriften für die Electronmikroskopie. Veb Gustav Fischer Verlag, Jena
19. Goncalves EC, Johnson JV, Rathinasabapathi B (2013) Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29. Planta 238:895–906. doi:10.1007/s00425-013-1946-5
20. Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10:1592–1606. doi:10.1128/EC.05242-11
21. Gorelova O, Kosevich I, Baulina O, Fedorenko T, Torshkhoeva A, Lobakova E (2009) Associations between the White Sea invertebrates and oxygen-evolving phototrophic microorganisms. Mosc Univ Biol Sci Bull 64:16–22
22. Gorelova O, Baulina O, Solovchenko A, Fedorenko T, Kravtsova T, Chivkunova O, Koksharova O, Lobakova E (2012) Green microalgae from associations with White Sea invertebrates. Microbiol (Mikrobiologiya) 81:505–507. doi:10.1134/S002626171204008X
23. Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Heidelberg, pp 1–24
24. Hockin NL, Mock T, Mulholland F, Kopriva S, Malin G (2012) The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol 158:299–312. doi:10.1104/pp.111.184333
25. Hüner NP, Bode R, Dahal K, Hollis L, Rosso D, Krol M, Ivanov AG (2012). Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Sci 3: article 255. doi: 10.3389/fpls.2012.00255
26. Johnson MP, Brain AP, Ruban AV (2011) Changes in thylakoid membrane thickness associated with the reorganization of photosystem II light harvesting complexes during photoprotective energy dissipation. Plant Signal Behav 6:1386–1390. doi:10.4161/psb.6.9.16503
27. Kates M (1986) Techniques of lipidology: Isolation, analysis and identification of lipids. Elsevier, Amsterdam
28. Khozin-Goldberg I, Shrestha P, Cohen Z (2005) Mobilization of arachidonyl moieties from triacylglycerols into chloroplastic lipids following recovery from nitrogen starvation of the microalga Parietochloris incisa. Biochim Biophys Acta 1738:63–71. doi:10.1016/j.bbalip.2005.09.005
29. Khozin-Goldberg I, Solovchenko A, Pal D, Cohen Z, Boussiba S (2013) Omega-3 and omega-6 LC-PUFA from photosynthetic microalgae: studies on Parietochloris incisa and Nannochloropsis sp. In: Catala A (ed) Polyunsaturated fatty acids: sources, antioxidant properties and health benefits. Nova Science Publishers, Hauppauge, pp 1–22
30. Li Y, Han D, Sommerfeld M, Hu Q (2011) Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour Technol 102:123–129. doi:10.1016/j.biortech.2010.06.036
31. Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo M-H, Benning C (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24:4670–4686. doi:10.1105/tpc.112.105106
32. Lourenço SO, Barbarino E, Marquez UML, Aidar E (1998) Distribution of intracellular nitrogen in marine microalgae: basis for the calculation of specific nitrogen-to-protein conversion factors. J Phycol 34:798–811
33. Majeran W, Olive J, Drapier D, Vallon O, Wollman F-A (2001) The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol 126:421–433. doi:10.1104/pp.126.1.421
34. Maxwell K, Johnson G (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659
35. McKay RML, Gibbs Sarah P, Vaughn KC (1991) RuBisCo activase is present in the pyrenoid of green algae. Protoplasma 162:38–45
36. Merzlyak M, Chivkunova O, Gorelova O, Reshetnikova I, Solovchenko A, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43:833–843. doi:10.1111/j.1529-8817.2007.00375.x
37. Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochem 75:50–59. doi:10.1016/j.phytochem.2011.12.007
38. Muller-Parker G, Lee KW, Cook CB (1996) Changes in the ultrastructure of symbiotic zooxanthellae (Symbiodinium sp., Dinophyceae) in fed and starved sea anemones maintained under high and low light. J Phycol 32:987–994
39. Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. PNAS 111:5042–5047. doi:10.1073/pnas.1322494111
40. Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11:4266–4273. doi:10.1002/pmic.201100114
41. Přibyl P, Cepák V, Zachleder V (2012) Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 94:549–561. doi:10.1007/s00253-012-3915-5
42. Přibyl P, Cepák V, Zachleder V (2013) Production of lipids and formation and mobilization of lipid bodies in Chlorella vulgaris. J Appl Phycol 25:545–553. doi:10.1007/s10811-012-9889-y
43. Reynolds E (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
44. Rhiel E, Mörschel E, Wehrmeyer W (1985) Correlation of pigment deprivation and ultrastructural organization of thylakoid membranes in Cryptomonas maculata following nutrient deficiency. Protoplasma 129:62–73
45. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. doi:10.1099/00221287-111-1-1
46. Roessler PG (1988) Effects of silicon deficiency on lipid composition and metabolism in the diatom Cyclotella cryptica. J Phycol 24:394–400. doi:10.1111/j.1529-8817.1988.tb04482.x
47. Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal E, Finazzi G, Morosinotto T (2013) The response of Nannochloropsis gaditana to nitrogen starvation Includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell 12:665–676. doi:10.1128/EC.00363-12
48. Sinetova M, Markelova A, Los D (2006) The effect of nitrogen starvation on the ultrastructure and pigment composition of chloroplasts in the acidothermophilic microalga Galdieria sulphuraria. Russ J Plant Physiol 53:153–162. doi:10.1134/S1021443706020026
49. Skjånes K, Rebours C, Lindblad P (2013) Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process. Crit Rev Biotechnol 33:172–215. doi:10.3109/07388551.2012.681625
50. Solovchenko A (2012) Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses. Russ J Plant Physiol 59:167–176. doi:10.1134/S1021443712020161
51. Solovchenko A, Khozin-Goldberg I, Cohen Z, Merzlyak M (2009) Carotenoid-to-chlorophyll ratio as a proxy for assay of total fatty acids and arachidonic acid content in the green microalga Parietochloris incisa. J Appl Phycol 21:361–366. doi:10.1134/S1021443713030138
52. Solovchenko A, Merzlyak M, Khozin-Goldberg I, Cohen Z, Boussiba S (2010) Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in Δ5 desaturase by nitrogen starvation and high light. J Phycol 46:763–772. doi:10.1111/j.1529-8817.2010.00849.x
53. Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-induced changes in optical properties, pigment and fatty acid content of Nannochloropsis sp.: implications for non-destructive assay of total fatty acids. Mar Biotechnol 13:527–535. doi:10.1007/s10126-010-9323-x
54. Solovchenko A, Chivkunova O, Semenova L, Selyakh I, Shcherbakov P, Karpova E, Lobakova E (2013a) Stress-induced changes in pigment and fatty acid content in the microalga Desmodesmus sp.isolated from a White Sea hydroid. Russ J Plant Physiol 60:313–321
55. Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013b) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a Δ5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182. doi:10.1016/j.algal.2013.01.010
56. Subramanian S, Barry AN, Pieris S, Sayre RT (2013) Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production. Biotechnol Biofuels 6: article 150. http://www.biotechnologyforbiofuels.com/content/6/1/1
57. Topf J, Gong H, Timberg R, Mets L, Ohad I (1992) Thylakoid membrane energization and swelling in photoinhibited Chlamydomonas cells is prevented in mutants unable to perform cyclic electron flow. Photosynth Res 32:59–69
58. Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868. doi:10.1128/EC.00272-09
59. Wellburn A (1994) The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. doi:10.1016/S0176-1617(11)81192-2
60. Yang Z-K, Niu Y-F, Ma Y-H, Xue J, Zhang M-H, Yang W-D, Liu J-S, Lu S-H, Guan Y, Li H-Y (2013). Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels 6: article 67. http://www.biotechnologyforbiofuels.com/content/6/1/6
61. Zachleder V, Brányiková I (2014) Starch overproduction by means of algae. In: Bajpai R, Prokop A, Zappi M (eds) Algal biorefineries. Springer, Dordrecht, pp 217–240